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Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Contents lists available at ScienceDirect
Journal of Experimental Marine Biology and Ecology
journal homepage: www.elsevier.com/locate/jembe
Impact of round goby on native invertebrate communities - An
experimental field study
Christina Henseler a, b, *, Daniel Oesterwind b, Paul Kotterba b, Marie C. Nordström a,
Martin Snickars a, Anna Törnroos a, Erik Bonsdorff a
a
Environmental and Marine Biology, Åbo Akademi University, Artillerigatan 6, Biocity, 20520 Åbo, Finland
b
Thünen Institute of Baltic Sea Fisheries, Alter Hafen Süd 2, 18069 Rostock, Germany
A R T I C L E I N F O A B S T R A C T
Keywords: This experimental field study provides first insights into the impact of a widely spread non-native fish species,
Biological invasion round goby Neogobius melanostomus (Pallas 1814), on the diversity of native epifaunal macroinvertebrate com
Cage experiment munities in the Baltic Sea. A cage experiment was conducted in a macrophyte habitat in the Åland islands located
Macroinvertebrate community
in the northern Baltic Sea. Round gobies (13.5 ± 0.8 cm) affected macroinvertebrate biodiversity from a taxo
Neogobius melanostomus
nomic and a trait-based point of view. Specifically, round goby decreased overall abundance, biomass and taxon
Baltic Sea
richness of epifaunal invertebrates. Additionally, taxonomic and trait-based composition were affected, as the
gobies reduced abundances of common bivalve (Cerastoderma spp. and Mytilus sp.) and gastropod species
(Hydrobia spp.), and thereby modified the relative trait composition of the invertebrate assemblages. Round
gobies consumed mainly larger epifaunal individuals leading to an overall decrease in invertebrate body size.
Such alterations in taxonomic and trait-based diversity and composition of invertebrate communities through
round goby predation may have implications for native fish species and other trophic levels in the respective food
webs through food competition and trophic cascades. Round gobies might therefore affect ecosystem processes in
invaded areas, and thus influence ecosystem functioning and services.
1. Introduction ecosystem services are mostly interpreted as negative (Charles and
Dukes, 2007). Nevertheless, the impact of non-native organisms in
Non-native organisms can have severe ecological impacts in invaded invaded ecosystems is complex and context-dependent, amongst others,
areas at a species-, community-, as well as an ecosystem-level. Effects of determined by both the trophic and functional group of the invader and
non-native species on the biodiversity of native communities can be both the native community (Ricciardi et al., 2013; Thomsen et al., 2014).
negative and positive, and manifest through direct biological in Whereas non-native species negatively affect the biodiversity of com
teractions such as predation, competition and grazing, but also indirect munities that have a similar trophic/functional level as the invader,
impacts through the modification of hydrographic variables and habi impacts on higher trophic levels and different functional groups are
tats (Gallardo et al., 2016). Since the biodiversity of communities, generally positive (Thomsen et al., 2014).
including species abundance, richness and trait properties, are closely The round goby (Neogobius melanostomus [Pallas 1814]) represents a
linked to ecosystem processes, non-native organisms can affect the successful invader that has colonized numerous habitats worldwide.
functioning of food webs and entire ecosystems and therefore also Originating from the Ponto-Caspian region, it can be found in a large
ecosystem services (Chapin III et al., 2000; Gallardo et al., 2016; Tilman array of brackish and freshwater ecosystems, such as the Great Lakes in
et al., 1997). For instance, non-native ecosystem engineers in marine North America, the Baltic Sea, and several European river- and canal
and estuarine environments can strongly influence ecosystem functions systems like the Rhine and the Danube (Kornis et al., 2012; Kotta et al.,
by negatively affecting growth and metabolic rates of native organisms, 2016). Round goby has become an established component of local food
and positively affecting nutrient fluxes, sedimentation and decomposi webs in its non-native range (Herlevi et al., 2018; Oesterwind et al.,
tion (Guy-Haim et al., 2017). Consequences of species invasions for 2017) by feeding on a wide variety of macroinvertebrates and, less
* Corresponding author.
E-mail address: christina.henseler@thuenen.de (C. Henseler).
https://doi.org/10.1016/j.jembe.2021.151571
Received 5 October 2020; Received in revised form 19 March 2021; Accepted 22 April 2021
Available online 5 May 2021
0022-0981/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
commonly, other fish and their fry, concurrently serving as prey for native fish species and its prey organisms might be complex and
various organisms including predatory fish and birds (e.g. Almqvist context-dependent.
et al., 2010; Rakauskas et al., 2013; Skora and Rzeznik, 2001; Vašek Due to their predation on specific organisms, high round goby den
et al., 2014; Wiegleb et al., 2018). As round gobies can reach high sities may not only cause shifts in invertebrate community biodiversity
densities and increasingly dominate fish communities in invaded areas and composition, but also alter the functional properties of invaded
(e.g. Jůza et al., 2018; Sapota and Skóra, 2005), this species has ecosystems and thus influence ecosystem functioning, as has been
frequently been suspected to have an influence on native organisms and shown for non-native ecosystem engineers (Guy-Haim et al., 2017). This
their ecological functions. Round goby has, for instance, been connected could be the case if round gobies would negatively affect organisms with
to the decline of native fish species (Janssen and Jude, 2001; Jůza et al., a set of key traits that are strongly linked to ecosystem processes, leading
2018; van Kessel et al., 2016) and is assumed to be causing diet shifts in to an alteration in trait composition of local invertebrate communities
fish and birds (Skabeikis et al., 2019; Ustups et al., 2016). Lower trophic (cf. Chapin III et al., 2000. However, studies on the link between round
levels, such as macroinvertebrate communities, might be affected goby predation and trait properties of prey communities are lacking,
through direct predation (Barton et al., 2005; Gallardo et al., 2016; although they give a more in-depth insight into the consequences of
Houghton and Janssen, 2015). round goby invasion for ecosystems and their functioning.
Several studies have investigated the impact of round gobies on The aim of this study is to examine the impact of round goby pre
native fish species, which comprises competition for food and space, dation on native epifaunal invertebrate communities in the Baltic Sea.
preying on fry and juveniles, and serving as food source for predatory By means of a field experiment, we study how round gobies affect the
fish (Hirsch et al., 2016). However, experimental studies examining how taxonomic and trait diversity and composition of invertebrate commu
round goby affects macroinvertebrate communities are surprisingly nities in a macrophyte habitat, where round gobies have established
scarce. Nurkse et al. (2018) studied the effects of round gobies on themselves in the local food web (Herlevi et al., 2018). Understanding
common benthic invertebrate species from the Baltic Sea in aquaria, the impact of non-native species may ultimately contribute to finding
discovering that this fish species is capable of significantly reducing adequate management strategies for newly colonized areas.
abundances of its prey organisms. Studies conducted under natural
conditions, i.e. field experiments, stem mostly from the Great Lakes, 2. Material and methods
where round goby impacts have been examined by means of cage ex
periments (Kornis et al., 2014; Kuhns and Berg, 1999; Mikl et al., 2017) 2.1. Study site
and by comparing invertebrate communities amongst sites where round
goby is present or absent (Kipp et al., 2012; Kipp and Ricciardi, 2012; To examine the impact of the non-native round goby on native
Krakowiak and Pennuto, 2008; Lederer et al., 2006). Results have shown invertebrate communities, a field experiment was carried out in a
that round gobies substantially alter invertebrate community structure macrophyte habitat in the northern Baltic Sea (Fig. 1) from 27 July until
by reducing densities of certain species, such as bivalves (e.g. zebra 7 September 2017. The experiment site was situated in the Åland ar
mussels Dreissena polymorpha), crustaceans, gastropods and chirono chipelago at the north-eastern coast of an island close to Mariehamn
mids. Yet, not all of these studies reported a significant impact of round (60◦ 3′ 15.84′′ N, 19◦ 57′ 52.2′′ E; salinity around 6; Fig. 1b). In the
goby on invertebrates, suggesting that interactions between this non- Åland Islands, the first round goby was caught in 2011 in the harbour of
Fig. 1. Map of the (A) Baltic Sea with the (B) Åland Islands located at the entrance of the Gulf of Bothnia. A red asterisk marks the location of the experiment site in
the Åland archipelago.
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C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Mariehamn (Herlevi et al., 2018). The macrophyte habitat was within
10 m proximity to shore in a softbottom area with sandy to muddy
sediment. Macrophyte and algae species in the habitat included Stuck
enia pectinata/Potamogeton pusillus, Chorda filum, Potamogeton perfoliatus
and Myriophyllum spp.. The experiment was conducted in 1.7 to 2.7 m
water depth in an area where round goby presence had already been
documented to avoid potentially contributing to a further spread of the
species.
2.2. Round goby collection and holding
To collect round gobies for the experiment, fishing was conducted
continuously over a time period of six weeks (20 July until 31 August
2017) before round gobies were used in the experiment, using baited
eelfykes (length: 10 m, height: 40 cm, mesh sizes: 11, 14 and 17 mm) in
the harbour of Mariehamn. During this time, gobies were held at den
sities of around 10 individuals in well‑oxygenated holding tanks (1 m
length x 1 m width x 60 cm height) at Husö Biological Station. The
bottom of the tanks was covered with sand, while stones, flowerpots and
pipes provided shelter for the fish. Tanks were subjected to ambient
natural light conditions and additional artificial light during daytime
(12 h artificial light during the day). Holding tanks were cleaned, and
the water was exchanged regularly (every two to three days). Sand-
filtered seawater was obtained directly from the bay near the station.
Water conditions (e.g. temperature, salinity, oxygen concentration)
therefore reflected ambient natural conditions, and were monitored
regularly (overall mean values ± SD for holding tanks: temperature =
16.8 ± 1.0 ◦ C, salinity = 5.3 ± 0.1, oxygen saturation = 97.1 ± 4.2%). Fig. 2. Illustration of the experimental design in the macrophyte habitat.
Gobies were fed once a day with a mix of live, natural food items i.e.
macroinvertebrates, such as amphipods and blue mussels, that naturally
density in the cages was therefore approximately seven individuals per
occur at the experiment site. Thus, round gobies were kept in aquarium
m2. Fish were sexed and measured for total length (TL) in the field
conditions resembling natural field conditions as closely as possible. Fish
directly before introducing them into the cages (mean size ± SD and
were left without feeding the day before including them in the cages.
female: male ratio = 13.5 ± 0.8 cm, 5:7). Round gobies were included in
the cages for one week, after which the invertebrate community was
2.3. Experimental design
sampled in all cages for the second time (Sampling 2). Due to poor
visibility, it was not possible to retrieve hiding and fast-moving gobies
To examine how round goby predation affects native invertebrates, a
from the cages for stomach content analyses without disturbing the
cage experiment was conducted, in which taxonomic and trait-based
sampling area i.e. the cage bottom and therefore compromising inver
diversity measures of invertebrate communities were compared be
tebrate samples. Additional to cage samples, invertebrates were sampled
tween cages including round gobies and cages excluding fish. The
in untreated areas at the experiment sites (Ambient samples, 6 repli
experiment was carried out by SCUBA diving. Round rubber tubs served
cates) to get an unbiased picture of the invertebrate community at the
as cages (volume = 65 l, height: 45 cm, diameter at the opening: 60 cm,
study site. These samples were taken simultaneously with the cage
diameter at the bottom: 45 cm, n = 12). Four big holes in the sides and
samples at Sampling 1 and Sampling 2. On each field day, hydrographic
another hole in the bottom of the tub were covered with a white nylon
conditions (temperature, salinity, pH, oxygen concentration) were
net (mesh size = 4.5 mm), which could be opened and closed at the
recorded at the experiment site.
bottom of the tub. At the study site, tubs were set upside down onto the
seafloor with their open side facing downwards (cage area: 0.28 m2).
Each cage was fastened to the bottom by a thick sand-filled fabric hose 2.4. Invertebrate community sampling
around the cage edges and attached with ropes to prevent cage dislo
cations and round goby escapes. Twelve cages were placed centrally in Sampling of invertebrates followed the procedure of Henseler et al.
the macrophyte habitat in a random order with a distance between 0.5 (2019) with slight modifications. Invertebrate epifauna was sampled by
and 3 m between any two cages. collecting all macrophyte and algae material including attached or
Total experiment time was six weeks starting with a four-week ganisms within a 25 × 12.5 cm area into net bags (mesh size: 0.5 mm).
adaptation period, during which no fish were inside the cages and no The two samples (at Sampling 1 and Sampling 2) were taken at opposite
fish could enter from the surrounding area (Fig. 2). The purpose of this sides within each cage (e.g. first sample taken at the northern side,
adaptation period was to standardize cages as best as possible by ac second one taken at the southern side of the cage). Invertebrate samples
counting for the effect the cages might have on the benthic invertebrate were sieved (mesh size: 0.5 mm) and stored in 70% Ethanol until further
community and the structure of the seafloor, and to allow invertebrate processing. Invertebrates were identified to the lowest possible taxo
recolonization of the cages. During these four weeks, cages were nomic group, counted and weighed. Some organism groups were too
inspected weekly for cleaning the outside of the nylon nets. After the light to be weighed, which is why the biomass presented here only takes
adaptation period, epifaunal invertebrate samples were taken in all into account weighable invertebrate taxa. For the trait analysis, the body
cages (Sampling 1; see below for sampling procedure). One week later, size of individual invertebrates was measured under a light microscope
round gobies were randomly included in respectively half of the cages to the nearest μm. When the number of individuals per taxonomic group
per habitat (Inclusion treatment, six replicates) whereas the other half was more than 50, body size was measured for a representative sub
remained empty (Exclusion Treatment, six replicates). For the Inclusion sample of at least 50 individuals. Invertebrate density and biomass were
treatment, two round gobies were placed into the cages. Round goby standardized to sample volume to allow a direct comparison of samples.
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C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Sample volume was measured with the water replacement method as the version 3.6.1 (R Core Team, 2019). Some samples were excluded from
volume of macrophyte and algae material (mean sample volume ± SD: the analysis due to handling problems resulting in five Inclusion repli
12.8 ± 11.3 cm3). cates at Sampling 1, and respectively five Inclusion and Exclusion rep
licates at Sampling 2. There were six replicates of the Exclusion
2.5. Invertebrate traits treatment at Sampling 1. Only invertebrate taxa that were present in at
least three samples were included in the analysis (cf. Supplement,
For the biological trait analysis of the invertebrate community, eight Table S1 for a complete species list).
categorical and one continuous traits were used (Table 1). Traits were To compare the diversity of invertebrate communities between
chosen to describe the fundamental ecology of organisms, considering Exclusion and Inclusion treatments, different taxonomic and trait-based
basic aspects of life-history including size, age, reproduction, feeding community measures were calculated. Taxonomic measures included
and morphology. Invertebrate traits and the construction of the species- invertebrate abundance and biomass, as well as the following indices:
trait matrix were adapted from Henseler et al. (2019). If body length was taxon richness, Pilou’s evenness and the Shannon index (calculated with
missing for a species in a sample due to non-intact individuals, the mean the vegan package; Oksanen et al., 2018). Trait indices - trait richness,
length of this species from all samples within the same treatment at the trait evenness and trait dispersion - were computed with the FD package
same sampling time (Sampling 1 or Sampling 2) was used. (Laliberté et al., 2014; Laliberté and Legendre, 2010). A more detailed
description of the FD (functional diversity) calculation can be found in
Henseler et al. (2019). Whereas trait richness refers to the number of
2.6. Data and statistical analysis
trait categories expressed in a community, i.e. the trait space taken by
species in a community, trait evenness describes the distribution of
All data analyses were conducted in the open source software R,
species abundances between expressed trait categories (described as
functional richness and evenness in Mason et al., 2005). Trait dispersion
Table 1 can be perceived as a measure for trait diversity, as it represents the
List of invertebrate traits (8 categorical, 1 continuous) and trait categories used spread of the community in multidimensional trait space, and is defined
for the biological trait analysis. Labels correspond to the trait categories shown
as the abundance weighted mean distance of species to their weighted
in Fig. 5. Table adapted from Henseler et al. (2019).
group centroid in trait space (described as functional dispersion in
Trait Category Label Relevance Laliberté and Legendre, 2010). To assess invertebrate community
Body size Continuous a
– Growth rate, productivity, structure, both taxonomic (based on log-transformed abundances) and
metabolism, feeding interactions trait composition were computed. Trait composition was based on
Longevity Very short (< 1 vsho Life cycle/lifespan, productivity
community-level weighted mean trait values (CWM), calculated by
yr)
Short (1–2 yrs) sho weighing expressed trait categories by relative abundances for each
Long (2–5 yrs) lon sample.
Very long (5–10 vlon Community measures of invertebrates (taxonomic and trait-based
yrs) indices and composition) were compared between treatments at Sam
Reproductive Annual episodic anep Reproduction, productivity
pling 1 and Sampling 2 (same approach as in Kornis et al., 2014). For
frequency Annual anpr
protracted indices, differences between Exclusion and Inclusion treatments were
Semelparous sem analysed with Linear Models (LM) using Type II Sum of Squares (car
Living habit Attached att Living environment, dispersal, package, Fox and Weisberg, 2011). LMs were conducted with indices as
Burrow dweller budw foraging mode
response variables, and treatment (2 levels: Exclusion and Inclusion)
Free free
Tube dweller tub
and sampling time (2 levels: Sampling 1 and Sampling 2) as fixed fac
Feeding position Suspension sus Food acquisition, feeding mode tors, including an interaction term of treatment and sampling time.
feeder Significant interaction terms indicate that the treatment effect differs
Surface feeder surf with sampling time (i.e. before and after round goby inclusion). In this
Sub-surface susurf
context, non-significant differences between treatments at Sampling 1
feeder
Selection feeder sel show that invertebrate communities were standardized sufficiently in all
Miner min cages before round gobies were included, whereas significant differ
Resource capture Cirri cirr Food acquisition, ences between treatments at Sampling 2 can be related to the effect of
method Jawed jaw complementary to Feeding
round gobies on invertebrate communities. Abundances were analysed
Net net position: summarize diet
Pharynx phar
with Generalized Linear Models (GLM) using Type II Sum of Squares
Radula rad including abundance count data as response variable and an offset with
Siphon siph the respective volume of each sample using a negative binomial distri
Movement type No movement nom Mobility, dispersal, ability to bution (MASS package; Venables and Ripley, 2002) and a log-link
Swimmer swim escape predation
function. For taxon richness, we used a quasipoisson distribution and
Rafter-drifter raft
Crawler crawl a log-link function. All other indices were modelled with the normal
Byssus threads byss distribution and log-transformed as needed to meet model assumptions.
Tube tube Assumptions of data normality and homogeneous variances were
Burrower burr checked by plotting residuals against fitted values. To compare indices
Body design Articulate art Body structure, protection
Bivalved biv against predation
between Exclusion and Inclusion treatments at Sampling 1 and 2, pair
Conical con wise post-hoc comparisons were conducted using the lsmeans function
Turbinate tur (lsmeans package; Lenth, 2016). To test for differences in taxonomic and
Vermiform ves trait composition between treatments for Sampling 1 and Sampling 2,
segmented
respectively, permutational multivariate ANOVAs (PERMANOVA) were
Vermiform veun
unsegmented conducted with 9999 permutations using the Bray-Curtis dissimilarity
Sociability Solitary sol Social behaviour for taxonomic composition, and the Gower distance for trait composi
Gregarious greg tion. To check if multivariate dispersions were homogeneous between
Aggregated agg treatments, a permutational test of multivariate dispersion (PERMDISP)
a
Obtained from individual species measurements from the samples. was applied prior to each PERMANOVA. Since PERMANOVA indicated a
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C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
significant result for the trait composition at Sampling 2, a SIMPER 3.2. Trait-based indices and composition of invertebrates
(similarity percentage) analysis was used to assess the dissimilarity be
tween treatments regarding their invertebrate community trait compo Trait indices (trait richness, trait evenness and trait dispersion) did
sition, and to identify which traits contributed most to this dissimilarity. not have a significant model interaction of treatment and sampling time
Since taxonomic composition showed significant differences between (p > 0.05; Table 2; Fig. 3). Thus, trait indices did not differ between
treatments at Sampling 2, abundances of specific species were analysed Exclusion and Inclusion cages at either of the sampling times. The
and compared between treatments. Only the most abundant species relative invertebrate trait composition based on weighted trait values
within a habitat (98% of the cumulative abundances) were compared differed significantly between treatments at Sampling 2 (p = 0.044;
between treatments, as they were well represented in the samples and Table 2; Fig. 5), whereas it was similar for Exclusion and Inclusion cages
therefore suitable for statistical analysis. To test whether invertebrate before round goby inclusion at Sampling 1 (p = 0.209; cf. Supplement,
communities were similar between Ambient samples and Exclusion/ Fig. S2 for trait composition based on absolute trait values). SIMPER
Inclusion cages before round goby inclusion, i.e. the starting point in results revealed an 18%-dissimilarity between invertebrate commu
cage and ambient communities was the same, taxonomic and trait-based nities from Exclusion and Inclusion cages at Sampling 2. The trait cat
indices and composition were statistically compared between Ambient egories explaining most of this dissimilarity were Body size, Resource
samples and treatments (Exclusion, Inclusion) at Sampling 1 using LMs capture method - siphon, Body design - bivalved and Living habit - attached
or GLMs. Maps were generated using the packages GISTools, rgdal, contributing together 29% to the between-treatment dissimilarity (cf.
raster and oceanmap (Bauer, 2018; Bivand et al., 2017; Brunsdon and Supplement, Table S4 for SIMPER results). Community-level weighted
Chen, 2014; Hijmans, 2017). mean values (CWM) of Body size were relatively smaller in the Inclusion
treatment than in the Exclusion treatment, whereas the other trait cat
3. Results egories had relatively higher values in the Inclusion cages (Fig. 5). Mean
Body Size based on absolute values of invertebrates was similar in
In total, 20 invertebrate species were found in the samples, of which Exclusion (2.6 ± 1.7 mm) and Inclusion (2.1 ± 1.3 mm) cages at Sam
17 were considered in the analysis (Supplement, Table S1). Invertebrate pling 1 before round goby inclusion (ANOVA: p = 0.266, F1,58 = 1.26).
communities did not differ between Ambient samples and Exclusion/ At Sampling 2, invertebrates were comparatively smaller in the Inclu
Inclusion treatments at Sampling 1 with respect to taxonomic or trait- sion (1.8 ± 0.8 mm) than in the Exclusion treatment (2.6 ± 1.9 mm;
based measures (indices and composition; analysis not shown; cf. ANOVA close to significant: p = 0.088, F1,52 = 3.02; Supplement,
Fig. 3), showing that invertebrate communities in the cages represen Fig. S3).
tatively reflected natural communities at the experiment start.
4. Discussion
3.1. Taxonomic indices and composition of invertebrates To examine the impact of a widely distributed, non-native fish spe
cies, round goby, on the biodiversity of epifaunal, native invertebrates, a
In the following section, we focus on the interaction effects of field experiment was conducted in the northern Baltic Sea. There was a
treatment and sampling time in the model results regarding taxonomic clear difference in taxonomic and trait properties of invertebrate com
and trait-based indices, as these provide the necessary information to munities between Exclusion and Inclusion treatments indicating that
evaluate round goby predation effects on invertebrate communities (cf. round goby predation affected invertebrate communities. This impact of
section “Data and statistical Analysis”; cf. Supplement, Table S2 and S3 round goby on the taxonomic and trait-based biodiversity of native or
for complete model results). Regarding the taxonomic invertebrate ganisms might have repercussions for ecosystem processes, and impair
community measures, a significant interaction between treatment and ecosystem functioning in invaded areas.
sampling time was found for total abundance (p = 0.010), biomass (p =
0.004) and taxon richness (p = 0.010), whereas no significant interac 4.1. Round goby impact on invertebrate communities regarding
tion existed for Pielou’s evenness and the Shannon index (p > 0.05; taxonomic measures
Table 2; Fig. 3). Post-hoc comparisons showed that abundance, biomass
and taxon richness were higher in the Exclusion than in the Inclusion Round goby affected the invertebrate community in the studied
treatment at Sampling 2 (p < 0.05; Exclusion vs. Inclusion [mean ± SD]: macrophyte habitat in the Åland Islands, both regarding taxonomic and
44,200.0 ± 38,745.8 vs. 5640.0 ± 3268.7 n/dm3; 159.9 ± 135.9 vs. 5.5 trait-based measures. In the presence of fish, total abundance and
± 3.8 g/dm3; 7 ± 1 vs. 4 ± 1 taxa), but they did not differ between biomass, as well as taxon richness of invertebrates were lower than in
treatments at Sampling 1 (p > 0.05). round goby absence, indicating that round goby predation negatively
Based on PERMANOVA results, the taxonomic composition of affected the taxonomic biodiversity of epifaunal macroinvertebrate
invertebrate communities was similar between treatments at Sampling 1 communities. Similar results have been found in experimental studies
(p = 0.09), but differed between Exclusion and Inclusion at Sampling 2 from the Great Lakes area, which report decreased invertebrate densities
(p = 0.008; Table 2). Consequently, abundances of specific invertebrate (abundance and biomass) and lower Shannon diversity due to round
taxa were analysed including Amphibalanus improvisus, Cerastoderma goby (Kipp and Ricciardi, 2012; Krakowiak and Pennuto, 2008; Kuhns
spp., Hydrobia spp. and Mytilus sp., which contributed 98% to the cu and Berg, 1999; Lederer et al., 2006). Taxonomic composition of in
mulative abundance of all samples (cf. Supplement, Fig. S1 for abun vertebrates differed between Exclusion and Inclusion cages after fish
dances of all species). Models on the abundances of Cerastoderma spp., inclusion, suggesting that round gobies also had an effect on community
Hydrobia spp. and Mytilus sp. showed a significant interaction between composition based on species abundances. Specifically, abundances of
treatment and sampling time (p < 0.05; Table 3; Fig. 4), whereas the Cerastoderma spp., Hydrobia spp. and Mytilus sp. were lower in the
interaction was close to significant for Amphibalanus improvisus (p = presence of round gobies, implying that these species were targeted as
0.054). Post-hoc comparisons revealed no difference between treat prey organisms. This result is not surprising, as round gobies naturally
ments at Sampling 1 for any of the invertebrate taxa (p > 0.05). How feed on these bivalve and gastropod species in different parts of the
ever, abundances were lower in the Inclusion than in the Exclusion Baltic Sea (Järv et al., 2011; Karlson et al., 2007; Oesterwind et al.,
treatment at Sampling 2 for Cerastoderma spp. (p < 0.001; 911.1 ± 859.4 2017; Rakauskas et al., 2008). Round gobies generally undergo an
vs. 18,838.9 ± 15,171.1 n/dm3), Hydrobia spp. (p = 0.017; 860.0 ± ontogenetic diet shift comprising an increasing incorporation of mol
589.9 vs. 2773.3 ± 1676.9 n/dm3) and Mytilus sp. (p = 0.014; 3626.7 ± luscs in the diet with increasing body size. Correspondingly, individuals
2463.0 vs. 21,525.6 ± 26,568.7 n/dm3). within the size range used in the cage experiment (13.5 ± 0.8 cm) feed
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C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Fig. 3. Taxonomic and trait indices of the invertebrate community: (A) abundance, (B) biomass, (C) taxon richness, (D) Pielou’s evenness, (E) Shannon index, (F)
trait richness, (G) trait evenness and (H) trait dispersion. Indices are shown for Sampling 1 (before round goby inclusion) and Sampling 2 (after round goby inclusion)
for Ambient samples, Exclusion and Inclusion treatments. Box whiskers indicate the lowest/highest values still within 1.5 times the interquartile range from the box
and therefore represent minima and maxima when no outliers exist. Outliers are displayed as dots and mean values as diamonds. Asterisk indicate significant
differences between Exclusion and Inclusion treatments. Significance levels lie at 0.05.
6C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Table 2 on molluscs to a large extent (Hempel et al., 2019; Karlson et al., 2007;
Comparison of taxonomic and trait-based indices and composition of inverte Skabeikis and Lesutienė, 2015; Skora and Rzeznik, 2001). Round gobies
brate communities between treatments (Exclusion and Inclusion) and sampling are assumed to possess an opportunistic feeding strategy, preying on
times (Sampling 1 and Sampling 2) by means of Generalized/Linear models and organisms that are available in high abundances (Borcherding et al.,
F-tests for univariate analyses and PERMANOVA for multivariate analyses. Only 2013; Brandner et al., 2013), which corroborates our findings. Cera
results of the interaction effects of treatment and sampling time are shown. For
stoderma spp., Hydrobia spp. and Mytilus sp. were the most abundant
complete model results, cf. Table S2 in the Supplementary Material.
invertebrate taxa in the cages in the beginning and at the end of the
Variable df F p experiment, as well as in the Ambient samples (cf. Supplement, Fig. S1),
Abundance 1 1.61 0.222 indicating that round gobies in our experiment fed on the invertebrate
Biomass 1 0.13 0.720 species with the highest availability. Therefore, it is most likely that they
Taxon richness 1 0.73 0.405
also prey on these organisms under natural conditions at the study site.
Pielou’s evenness 1 2.70 0.119
Shannon index 1 2.29 0.149 The effects of this non-native fish species might accordingly be strongest
Trait richness 1 0 0.999 for taxa dominant in a specific environment. While the impact of round
Trait evenness 1 0.47 0.505 goby on invertebrate abundance and biomass in our study is likely a
Trait dispersion 1 2.38 0.142 result of direct predation on the most abundant taxa, the decline in taxon
Taxonomic composition
richness might additionally be linked to a decrease in habitat structure
treatment at Sampling 1 9 0.12 0.953
treatment at Sampling 2 10 1.90 0.101 and food availability, which is provided by bivalves, as suggested by
Trait composition Lederer et al. (2006). Due to a previous lack of experimental field studies
treatment at Sampling 1 9 0.52 0.853 on round goby impact from the Baltic Sea, a comparison of our results to
treatment at Sampling 2 10 1.60 0.183
findings from the same invaded region is not possible. However, lab
studies conducted in the Baltic Sea have documented that round gobies
are able to reduce abundances of gammarids and bivalves, including
Table 3 Macoma balthica and Mytilus sp. (Nurkse et al., 2018), which partly fits
Comparison of abundances of the most abundant invertebrate species the results of our experiment. Experimental studies from the Great Lakes
(contributing 98% to the cumulative abundance of all samples) between treat found a negative effect of round goby predation on the density of certain
ments (Exclusion and Inclusion) and sampling times (Sampling 1 and Sampling
invertebrate taxa, such as gastropods, bivalves (dreissenids) and, to a
2) by means of Generalized Linear models and F-tests. Only results of the
large extent also, insects (Kipp and Ricciardi, 2012; Krakowiak and
interaction effects of treatment and sampling time are shown. For complete
model results, cf. Table S3 in the Supplementary Material. Pennuto, 2008; Kuhns and Berg, 1999; Lederer et al., 2006). As round
gobies seem to have an impact on invertebrate taxa with the highest
Species df F p
availability in the environment, their effect in an ecosystem may be
Amphibalanus improvisus 1 4.30 0.054 context-dependent and vary conditional on dominating prey species in
Cerastoderma spp. 1 12.18 0.003*
invaded areas. Contrary to their impact on epifaunal invertebrates,
Hydrobia spp. 1 6.89 0.018*
Mytilus sp. 1 4.85 0.042* round gobies did not seem to affect infaunal macroinvertebrate com
munities in the same macrophyte habitat in Åland, based on a small-
scale pilot study (Henseler, unpublished results; cf. Supplement,
Table S5 for infaunal species considered in this study). Taxonomic
indices (total abundance, biomass, taxon richness, Pielou’s evenness and
Fig. 4. Mean abundances and standard deviation of
invertebrate species that were compared statistically
between treatments: Amphibalanus improvisus (A.i.),
Cerastoderma spp. (C.spp.), Hydrobia spp. (H.spp.),
Mytilus sp. (M.sp.). Abundances are shown for (A)
Sampling 1 (before round goby inclusion) and (B)
Sampling 2 (after round goby inclusion), for Ambient
samples, as well as for the Exclusion and Inclusion
treatments. Asterisk indicate significant differences
between Exclusion and Inclusion treatments, and
“NS” point out non-significant differences. Signifi
cance levels lie at 0.05.
7C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
Fig. 5. Relative trait composition displayed as community-weighted means (CWM) i.e. weighted trait values, of the invertebrate community. CWMs are shown for
(A) and (B) Sampling 1 (before round goby inclusion) and (C) and (D) Sampling 2 (after round goby inclusion) for the Exclusion (left column) and Inclusion (right
column) treatments. Colour coding refers to the different traits. For label descriptions, cf. Table 1. Body Size was excluded from the plots due to disproportionally
large CWM values.
Shannon index) and composition of infaunal invertebrate communities on CWM i.e. weighted trait values), which differed between Exclusion
did not differ between round goby presence and absence. This indicates and Inclusion treatments at the end of the experiment. The overall
that the predation effect of round gobies is possibly higher for inverte dissimilarity between the treatments was, however, comparatively low
brate epifauna than for infaunal communities, at least under small-scale (18%). Nonetheless, the traits most responsible for this difference can be
experimental conditions. However, since other experimental studies (e. directly linked to the invertebrate species, which were most affected by
g. from the Great Lakes; see references above) have only considered the round gobies regarding their abundances. Whereas Resource capture
impact of round goby on epifaunal prey communities, this aspect re method - siphon and Body design - bivalved are associated with bivalves,
quires further investigation. Living habit - attached is additionally expressed by Mytilus sp.. Thus,
round goby had the highest impact on trait categories that are linked to
4.2. Round goby impact on invertebrate communities regarding trait- the taxa, which experienced an abundance decline through round goby
based measures predation. These trait categories had a higher contribution to the rela
tive trait composition in the Inclusion cages (Fig. 5), which can be
Round goby predation did not only affect the taxonomic structure of explained by the overall reduced taxon richness, making the traits of the
the invertebrate community, but also the trait-based composition (based most abundant organisms, Cerastoderma spp., Hydrobia spp. and Mytilus
8C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
sp., dominate even more in the community. The expression of trait this species on invertebrate communities could accordingly be weaker or
categories based on absolute trait values (i.e. not weighted by relative stronger. Another aspect worth considering in the impact assessment of
abundances for each sample) was overall lower in the Inclusion than in non-native species is the health status of individuals in a population. In a
the Exclusion treatment (Supplement, Fig. S2), implying that round parallel experiment with a similar set-up conducted at the German coast
goby also affected the absolute expression of traits in the experiment. (data not shown), round gobies were in a poor body condition displaying
Thus, round goby predation reduces the overall contribution of inver infected spots on the skin and caudal fins (Supplement, Fig. S4). Addi
tebrate traits to ecosystem processes (due to changes in absolute trait tionally, many dead individuals were observed in the field. This was
expression) potentially leading to an overall decrease in ecosystem witnessed at various locations along the German coastline in addition to
functions (quantitative effect). Additionally, the relative contribution of Danish, Swedish and Estonian coastal waters (Jane Behrens and Redik
traits to these processes is altered (due to changes in relative trait Eschbaum, personal communication). One year later, round gobies in
expression) possibly causing a shift in magnitude of certain processes the Åland archipelago showed similar disease symptoms (personal
(qualitative effect). Round goby impacts on invertebrate communities observation) indicating a Baltic Sea wide infection of this non-native
might therefore have consequences for ecosystem functioning in species during the years 2017/2018. In the experiment in Germany,
invaded areas due to a modification in invertebrate trait expression there was no predation effect of round gobies on invertebrate commu
(Chapin III et al., 2000). The trait Body Size contributed most to the nities, which might potentially be linked to the poor body condition of
difference in relative trait composition of invertebrates between Exclu the fish, although this can only be speculated. Yet, impact studies should
sion and Inclusion cages, and was smaller in the presence of round go take into account body condition of invaders when evaluating their ef
bies (difference in mean size close to significant between treatments at fects on native organisms and ecosystems.
Sampling 2). Thus, round gobies fed on larger individuals indicating that Through their predation on native invertebrates, round gobies could
this fish species can affect the size structure of communities. This is in have an indirect impact on organisms of a similar trophic level i.e. native
line with findings from other invaded areas, where round gobies like fish species, feeding on the same organisms. As a successful invader,
wise decreased the size of prey organisms (Kipp et al., 2012; Kipp and round goby might be more efficient in preying on a wide spectrum of
Ricciardi, 2012; Mikl et al., 2017). On the other hand, lab studies organisms, as it has been shown in laboratory experiments in the Great
examining the impact of round goby feeding on different sizes of bi Lakes (Naddafi and Rudstam, 2014), making them competitively supe
valves generally show that round gobies (ca. 10–15 cm TL) select for rior to native fish species regarding predation rates. As round gobies
smaller individuals between 3 and 27 mm (Nurkse et al., 2016; Perello reduce abundances and overall body size of invertebrates, this could
et al., 2015; Schrandt et al., 2016; Schwartzbach et al., 2019). However, negatively affect native fish species in areas of high round goby density.
invertebrates in our experiment were generally rather small (overall size Availability of invertebrates is likely lower and mostly small, possibly
range of invertebrates in the macrophyte habitat: 0.4–12.0 mm; Sup juvenile, individuals will prevail in invaded areas, which might be
plement, Fig. S3) and thus still lie within the documented preferred size energetically less profitable prey for native fish. In the Baltic Sea,
range. As body size plays a significant role in food webs and ecological flounder Platichthys spp. represents one native species, which might
processes through its link to, amongst others, growth and metabolic experience food competition through round goby due to diet overlap.
rates, productivity and mortality (Brose et al., 2017; Brown et al., 2004; Flounder feeds on similar prey organisms as round goby, including bi
Woodward et al., 2005), the alteration of invertebrate size structure valves (Macoma balthica, Mytilus sp.) and gastropods (Hydrobia spp.)
through round gobies could have implications for ecosystem functioning (Järv et al., 2011; Karlson et al., 2007), which belong to the species
in invaded regions. Yet, it has to be considered that natural round goby affected most in our cage experiment, suggesting that round goby might
populations also contain smaller individuals feeding on other, i.e. reduce food availability for flounder.
smaller, invertebrate sizes than fish in this experiment. This might result Besides their impact on native invertebrate and fish communities,
in an equal predation pressure for smaller and larger invertebrates under round gobies might affect other trophic levels, by inducing trophic
natural conditions. Hence, the main effect of round goby predation in cascades. By means of intense predation on invertebrate grazers, like
natural systems might rather manifest through an overall abundance small gastropods, high fish abundances can cause increased filamentous
reduction than through a shift in the size structure of native invertebrate algal growth (Eriksson et al., 2009; Korpinen et al., 2007). Accordingly,
communities. high round goby densities have been linked to increased benthic algal
Round gobies are generally documented to favour structured rocky biomass and chlorophyll-a concentrations, presumably through their
or stone habitats (e.g. Ramler and Keckeis, 2020; Ray and Corkum, consumption of grazing invertebrates (Kipp and Ricciardi, 2012; Kuhns
2001; Sapota and Skóra, 2005). Yet, high round goby abundances have and Berg, 1999). In our study, round gobies decreased abundances of
been found in a variety of other habitats (Kornis et al., 2012), under Hydrobia spp., which is a grazing gastropod, expressing the traits Feeding
lining the broad habitat use of this species. For instance, round goby position - surface feeder and Resource capture method - radula. The CWM-
presence in vegetated habitats on softbottom is known from the Baltic values of these categories were lower in the Inclusion than in the
Sea, the Great Lakes and the Caspian Sea (Bogutskaya et al., 2004; Exclusion treatment after fish inclusion at Sampling 2 (Fig. 5; Supple
Cooper et al., 2009; Cooper et al., 2007; Henseler et al., 2020; Jude and ment, Table S4), indicating that invertebrate grazing might decline in
DeBoe, 1996). Additionally, at our study site, round gobies were the presence of round gobies, potentially leading to increased opportu
observed in high numbers in the macrophyte habitat, rendering it nistic algae growth in coastal areas invaded by this fish species. This
appropriate to conduct this experiment in a vegetated area, even if this could have implications for ecosystem functioning, and affect ecosystem
might not constitute the primary habitat of this fish species. services of coastal habitats, for example through increased filamentous
algal blooms.
4.3. Ecological implications of round goby predation
5. Conclusions
For our experiment, the number of round gobies included in the
cages was chosen to resemble abundances in nature. Densities of this This field experiment provides novel insights into the impact of a
species from the Danish and Polish coast in the Baltic Sea range from 1.9 non-native fish species, round goby, on the biodiversity of native mac
up to 30 individuals per m2 (Azour et al., 2015; Sapota, 2004; Sapota roinvertebrate communities in the Baltic Sea. Round gobies negatively
and Skóra, 2005). Round goby density in our experiment (7 per m2) lay affected abundance, biomass and taxon richness of epifaunal in
well within this reported abundance range, reflecting natural field vertebrates in a macrophyte habitat in the northern Baltic Sea, and had
conditions. Depending on whether round goby abundances are lower or an influence on taxonomic and trait-based composition. Abundances of
higher in a specific invaded area than in our study, predation impacts of common Baltic Sea bivalve and gastropod species were lower in round
9C. Henseler et al. Journal of Experimental Marine Biology and Ecology 541 (2021) 151571
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10.1016/j.limno.2012.08.003.
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The authors declare that they have no known competing financial Charles, H., Dukes, J.S., 2007. Impacts of invasive species on ecosystem services. In:
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the work reported in this paper. Cooper, M.J., Ruetz III, C.R., Uzarski, D.G., Burton, T.M., 2007. Distribution of round
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for providing excellent field work facilities and Nåtö Biological Station Gallardo, B., Clavero, M., Sánchez, M.I., Vilà, M., 2016. Global ecological impacts of
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Åland, and J. Heiler, D. Hellström, I. Hermansson, J. Holmberg, R. Arvanitidis, C., Como, S., Magni, P., Blight, A.J., Orav-Kotta, H., Somerfield, P.J.,
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brackish Kiel Canal. Mar. Biodivers. 49, 795–807. https://doi.org/10.1007/s12526-
from the European Union’s Horizon 2020 research and innovation 018-0854-0.
programme under the Marie Skłodowska-Curie grant agreement No Henseler, C., Nordström, M.C., Törnroos, A., Snickars, M., Pecuchet, L., Lindegren, M.,
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the Commission is not responsible for any use that may be made of the 226, 106272. https://doi.org/10.1016/j.ecss.2019.106272.
information it contains. MCN and EB acknowledge the Åbo Akademi Henseler, C., Kotterba, P., Bonsdorff, E., Nordström, M.C., Oesterwind, D., 2020. Habitat
University Foundation. AT received funding from the profiling area The utilization and feeding ecology of small round goby in a shallow brackish lagoon.
Mar. Biodivers. 50 https://doi.org/10.1007/s12526-020-01098-0.
Sea at Åbo Akademi University. Herlevi, H., Aarnio, K., Puntila-Dodd, R., Bonsdorff, E., 2018. The food web positioning
and trophic niche of the non-indigenous round goby: a comparison between two
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